Dynamics of Co-Transcriptional Pre-mRNA Folding Influences the Induction of Dystrophin Exon Skipping by Antisense Oligonucleotides
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{"title"=>"Dynamics of co-transcriptional pre-mRNA folding influences the induction of dystrophin exon skipping by antisense oligonucleotides", "type"=>"journal", "authors"=>[{"first_name"=>"Keng Boon", "last_name"=>"Wee", "scopus_author_id"=>"24460864900"}, {"first_name"=>"Zacharias Aloysius Dwi", "last_name"=>"Pramono", "scopus_author_id"=>"8679354300"}, {"first_name"=>"Jian Li", "last_name"=>"Wang", "scopus_author_id"=>"24460751300"}, {"first_name"=>"Karl F.", "last_name"=>"MacDorman", "scopus_author_id"=>"6602161453"}, {"first_name"=>"Poh San", "last_name"=>"Lai", "scopus_author_id"=>"7202946489"}, {"first_name"=>"Woon Chee", "last_name"=>"Yee", "scopus_author_id"=>"23571232500"}], "year"=>2008, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "doi"=>"10.1371/journal.pone.0001844", "pui"=>"351936468", "sgr"=>"46649087777", "pmid"=>"18365002", "scopus"=>"2-s2.0-46649087777"}, "id"=>"f95022b3-354b-3bce-b337-7c8a5d9f6076", "abstract"=>"Antisense oligonucleotides (AONs) mediated exon skipping offers potential therapy for Duchenne muscular dystrophy. However, the identification of effective AON target sites remains unsatisfactory for lack of a precise method to predict their binding accessibility. This study demonstrates the importance of co-transcriptional pre-mRNA folding in determining the accessibility of AON target sites for AON induction of selective exon skipping in DMD. Because transcription and splicing occur in tandem, AONs must bind to their target sites before splicing factors. Furthermore, co-transcriptional pre-mRNA folding forms transient secondary structures, which redistributes accessible binding sites. In our analysis, to approximate transcription elongation, a \"window of analysis\" that included the entire targeted exon was shifted one nucleotide at a time along the pre-mRNA. Possible co-transcriptional secondary structures were predicted using the sequence in each step of transcriptional analysis. A nucleotide was considered \"engaged\" if it formed a complementary base pairing in all predicted secondary structures of a particular step. Correlation of frequency and localisation of engaged nucleotides in AON target sites accounted for the performance (efficacy and efficiency) of 94% of 176 previously reported AONs. Four novel insights are inferred: (1) the lowest frequencies of engaged nucleotides are associated with the most efficient AONs; (2) engaged nucleotides at 3' or 5' ends of the target site attenuate AON performance more than at other sites; (3) the performance of longer AONs is less attenuated by engaged nucleotides at 3' or 5' ends of the target site compared to shorter AONs; (4) engaged nucleotides at 3' end of a short target site attenuates AON efficiency more than at 5' end.", "link"=>"http://www.mendeley.com/research/dynamics-cotranscriptional-premrna-folding-influences-induction-dystrophin-exon-skipping-antisense-o", "reader_count"=>26, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>1, "Other"=>1, "Student > Master"=>2, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>1, "Other"=>1, "Student > Master"=>2, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>18, "Medicine and Dentistry"=>1, "Physics and Astronomy"=>1, "Chemistry"=>1, "Social Sciences"=>2, "Computer Science"=>1, "Unspecified"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>18}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United States"=>2, "France"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/935003"], "description"=>"<p>(A) to (C) For every example, the incidences of <i>engaged</i> nucleotides at each step of transcriptional analysis for all nucleotide in target sites of (++), (+) and (−) AONs were depicted.</p>", "links"=>[], "tags"=>["examples", "scores", "correlate", "aon", "efficacy", "compared"], "article_id"=>605442, "categories"=>["Biological Sciences", "Infectious Diseases", "Computational Biology"], "users"=>["Keng Boon Wee", "Zacharias Aloysius Dwi Pramono", "Jian Li Wang", "Karl F. MacDorman", "Poh San Lai", "Woon Chee Yee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001844.g006", "stats"=>{"downloads"=>2, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Three_examples_for_where_only_the_fourth_level_scores_can_correlate_AON_efficacy_and_efficiency_compared_to_third_level_scores_/605442", "title"=>"Three examples for where only the fourth level scores can correlate AON efficacy and efficiency compared to third level scores.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-03-26 01:30:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/934525"], "description"=>"<p>To approximate the transcription elongation process, a “window of analysis” is shifted one nucleotide at a time along the pre-mRNA sequence towards the 3′ end, beginning with the 3′ end of the exon targeted to be skipped at the window's 3′ end and stopping when the 5′ end of the targeted exon reaches the 5′ end of the window. Each window of analysis corresponds to a step of transcriptional analysis at which the possible secondary structures of its sequence were predicted.</p>", "links"=>[], "tags"=>["transcriptional", "elongation"], "article_id"=>604966, "categories"=>["Biological Sciences", "Infectious Diseases", "Computational Biology"], "users"=>["Keng Boon Wee", "Zacharias Aloysius Dwi Pramono", "Jian Li Wang", "Karl F. MacDorman", "Poh San Lai", "Woon Chee Yee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001844.g001", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Approximation_of_the_transcriptional_elongation_process_of_pre_mRNA_/604966", "title"=>"Approximation of the transcriptional elongation process of pre-mRNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-03-26 01:22:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/934907"], "description"=>"<p>(A) Box-plots for scores of groups of 3 nucleotides meeting criterion of analysis in target sites of (++) AONs, (+) AONs and (−) AONs of Set A, and of (++) AONs of Set B (***). (B) Box-plots for scores of groups of 4 nucleotides meeting criterion of analysis in target sites of both (+) and (−) AONs of Set A.</p>", "links"=>[], "tags"=>["scores"], "article_id"=>605353, "categories"=>["Biological Sciences", "Infectious Diseases", "Computational Biology"], "users"=>["Keng Boon Wee", "Zacharias Aloysius Dwi Pramono", "Jian Li Wang", "Karl F. MacDorman", "Poh San Lai", "Woon Chee Yee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001844.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Box_plots_for_each_of_the_fourth_level_scores_L4_AVG_L4_AND_and_L4_OR_/605353", "title"=>"Box-plots for each of the fourth level scores <i>L4_AVG, L4_AND</i> and <i>L4_OR.</i>", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-03-26 01:29:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/935077"], "description"=>"<p>The left panel shows the RT-PCR analysis of dystrophin mRNA treated with novelAON57 at concentrations of 100nM, 200nM and 400nM of AONs. For every AON concentration, the relative percentage of total transcripts (average value of duplicate transfections) with skipping of the targeted exon is given below the lanes. The middle panel indicates the relative position of the novel AONs with respect to published AONs. The right panel plots the <i>co-transcriptional</i> binding accessibility of the novel AON target sites, wherein the horizontal axis denotes sequential steps of transcriptional analysis and the vertical axis denotes numbered nucleotides within the AON target site. At each step of transcriptional analysis, nucleotides in the target site that are <i>engaged</i> are depicted as a black dot in the plot.</p>", "links"=>[], "tags"=>["aon", "targeting", "exon"], "article_id"=>605515, "categories"=>["Biological Sciences", "Infectious Diseases", "Computational Biology"], "users"=>["Keng Boon Wee", "Zacharias Aloysius Dwi Pramono", "Jian Li Wang", "Karl F. MacDorman", "Poh San Lai", "Woon Chee Yee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001844.g007", "stats"=>{"downloads"=>4, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_efficiency_of_a_novel_AON_targeting_exon_57_/605515", "title"=>"The efficiency of a novel AON targeting exon 57.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-03-26 01:31:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/934750"], "description"=>"<p>The quartiles (Q1, median and Q3) of the normalized first level scores (<i><u>L1</u></i>), and normalized third level scores (<i><u>L3</u></i>) for target sites of AONS in every AON grade of (A) Set A and (B) Set B are plotted. The units for all the vertical axes are in percentages.</p>", "links"=>[], "tags"=>["normalized"], "article_id"=>605197, "categories"=>["Biological Sciences", "Infectious Diseases", "Computational Biology"], "users"=>["Keng Boon Wee", "Zacharias Aloysius Dwi Pramono", "Jian Li Wang", "Karl F. MacDorman", "Poh San Lai", "Woon Chee Yee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001844.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quartiles_of_the_normalized_first_and_third_level_scores_/605197", "title"=>"Quartiles of the normalized first and third level scores.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-03-26 01:26:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/934692"], "description"=>"<p>In the above illustration, the horizontal axis denotes sequential steps of transcriptional analysis while the vertical axis denotes numbered nucleotides within the AON target site. At each step of transcriptional analysis, nucleotides in the target site that are <i>engaged</i> are depicted as a black dot in the plot. The calculations of the fourth level scores, <i>L4_OR</i> and <i>L4_AND</i>, are illustrated (refer to main text for details).</p>", "links"=>[], "tags"=>["nucleotides", "transcriptional"], "article_id"=>605136, "categories"=>["Biological Sciences", "Infectious Diseases", "Computational Biology"], "users"=>["Keng Boon Wee", "Zacharias Aloysius Dwi Pramono", "Jian Li Wang", "Karl F. MacDorman", "Poh San Lai", "Woon Chee Yee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001844.g003", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Occurrences_of_engaged_nucleotides_at_each_step_of_transcriptional_analysis_/605136", "title"=>"Occurrences of <i>engaged</i> nucleotides at each step of transcriptional analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-03-26 01:25:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/935142"], "description"=>"<p>The second column states the two AON grades being tested. ‘/’ means that two grades of AONs are combined into a single grade for the test. In the second row, ‘1<sup>st</sup>’ and ‘2<sup>nd</sup>’ denote the first and second grades being tested (as indicated in the corresponding second column). The last column indicates whether the particular K-S test tests for efficacy and/or efficiency. Significant p-values are highlighted in bold and underlined. Test results for <b>(A)</b> AONs in Set A; and <b>(B)</b> AONs in Set B.</p>", "links"=>[], "tags"=>["k-s", "variables", "differentiating", "efficacy"], "article_id"=>605587, "categories"=>["Biological Sciences", "Infectious Diseases", "Computational Biology"], "users"=>["Keng Boon Wee", "Zacharias Aloysius Dwi Pramono", "Jian Li Wang", "Karl F. MacDorman", "Poh San Lai", "Woon Chee Yee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001844.t001", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_p_values_for_K_S_tests_using_the_first_level_score_L1_and_third_level_score_L3_as_test_variables_for_differentiating_the_efficacy_and_or_efficiency_of_AONs_/605587", "title"=>"p-values for K-S tests using the first level score (<i>L1</i>) and third level score (<i>L3</i>) as test variables for differentiating the efficacy and/or efficiency of AONs.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-03-26 01:33:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/935177"], "description"=>"<p>Only tests with significant p-values were shown. <b>(A)</b> Test data includes both 3′ and 5′ ends of AON target sites. <b>(B)</b> Test data consists of only 3′ end of AON target sites. <b>(C)</b> Test data consists of only 5′ end of AON target sites. <b>(D)</b> 3′ vs. 5′ end of AON target sites.</p>", "links"=>[], "tags"=>["k-s", "scores"], "article_id"=>605622, "categories"=>["Biological Sciences", "Infectious Diseases", "Computational Biology"], "users"=>["Keng Boon Wee", "Zacharias Aloysius Dwi Pramono", "Jian Li Wang", "Karl F. MacDorman", "Poh San Lai", "Woon Chee Yee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001844.t002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_p_values_for_K_S_tests_using_the_fourth_level_scores_as_test_variables_/605622", "title"=>"p-values for K-S tests using the fourth level scores as test variables.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-03-26 01:33:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/934607"], "description"=>"<p>(A) to (C). This is to illustrate that multiple secondary structures of the targeted exon (drawn in green) are predicted in each step of transcriptional analysis, with some of the possible structural motifs shown here. For illustration purpose, a particular nucleotide (marked in red) within an AON target site (green line) is tracked. When this nucleotide is paired (denoted with *), it is not accessible for AON binding. If this nucleotide is paired in all predicted secondary structures, this nucleotide is defined as an <i>engaged</i> nucleotide at this particular step of transcriptional analysis (B).</p>", "links"=>[], "tags"=>["nucleotide", "transcriptional"], "article_id"=>605049, "categories"=>["Biological Sciences", "Infectious Diseases", "Computational Biology"], "users"=>["Keng Boon Wee", "Zacharias Aloysius Dwi Pramono", "Jian Li Wang", "Karl F. MacDorman", "Poh San Lai", "Woon Chee Yee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001844.g002", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Definition_of_an_engaged_nucleotide_in_a_particular_step_of_transcriptional_analysis_/605049", "title"=>"Definition of an <i>engaged</i> nucleotide in a particular step of transcriptional analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-03-26 01:24:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/460525", "https://ndownloader.figshare.com/files/460556", "https://ndownloader.figshare.com/files/460600", "https://ndownloader.figshare.com/files/460639", "https://ndownloader.figshare.com/files/460698", "https://ndownloader.figshare.com/files/460822", "https://ndownloader.figshare.com/files/461019", "https://ndownloader.figshare.com/files/461050"], "description"=>"<div><p>Antisense oligonucleotides (AONs) mediated exon skipping offers potential therapy for Duchenne muscular dystrophy. However, the identification of effective AON target sites remains unsatisfactory for lack of a precise method to predict their binding accessibility. This study demonstrates the importance of <em>co-transcriptional</em> pre-mRNA folding in determining the accessibility of AON target sites for AON induction of selective exon skipping in DMD. Because transcription and splicing occur in tandem, AONs must bind to their target sites before splicing factors. Furthermore, <em>co-transcriptional</em> pre-mRNA folding forms transient secondary structures, which redistributes accessible binding sites. In our analysis, to approximate transcription elongation, a “window of analysis” that included the entire targeted exon was shifted one nucleotide at a time along the pre-mRNA. Possible c<em>o-transcriptional</em> secondary structures were predicted using the sequence in each step of transcriptional analysis. A nucleotide was considered “<em>engaged</em>” if it formed a complementary base pairing in all predicted secondary structures of a particular step. Correlation of frequency and localisation of <em>engaged</em> nucleotides in AON target sites accounted for the performance (efficacy and efficiency) of 94% of 176 previously reported AONs. Four novel insights are inferred: (1) the lowest frequencies of <em>engaged</em> nucleotides are associated with the most efficient AONs; (2) <em>engaged</em> nucleotides at 3′ or 5′ ends of the target site attenuate AON performance more than at other sites; (3) the performance of longer AONs is less attenuated by <em>engaged</em> nucleotides at 3′ or 5′ ends of the target site compared to shorter AONs; (4) <em>engaged</em> nucleotides at 3′ end of a short target site attenuates AON efficiency more than at 5′ end.</p></div>", "links"=>[], "tags"=>["pre-mrna", "folding", "influences", "induction", "dystrophin", "exon", "skipping", "antisense", "oligonucleotides"], "article_id"=>150750, "categories"=>["Biological Sciences", "Cancer"], "users"=>["Keng Boon Wee", "Zacharias Aloysius Dwi Pramono", "Jian Li Wang", "Karl F. MacDorman", "Poh San Lai", "Woon Chee Yee"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0001844.s001", "https://dx.doi.org/10.1371/journal.pone.0001844.s002", "https://dx.doi.org/10.1371/journal.pone.0001844.s003", "https://dx.doi.org/10.1371/journal.pone.0001844.s004", "https://dx.doi.org/10.1371/journal.pone.0001844.s005", "https://dx.doi.org/10.1371/journal.pone.0001844.s006", "https://dx.doi.org/10.1371/journal.pone.0001844.s007", "https://dx.doi.org/10.1371/journal.pone.0001844.s008"], "stats"=>{"downloads"=>16, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Dynamics_of_Co_Transcriptional_Pre_mRNA_Folding_Influences_the_Induction_of_Dystrophin_Exon_Skipping_by_Antisense_Oligonucleotides/150750", "title"=>"Dynamics of <em>Co-Transcriptional</em> Pre-mRNA Folding Influences the Induction of Dystrophin Exon Skipping by Antisense Oligonucleotides", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-03-26 00:12:30"}

PMC Usage Stats | Further Information

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Relative Metric

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